<p>Rhizosphere microbiomes are critical for agricultural health, but how they are interactively shaped by management and host genetics in perennial systems remains largely unknown. Using an apple orchard system, we show that long-term agricultural management does not alter soil biodiversity but also selects for fundamentally opposing microbial life strategies. Our findings showed that organic management selects resource-decomposition specialists, while conventional management selects abiotic stress-tolerance and xenobiotic remediators. We found that this is achieved via taxonomic restructuring of functional guilds, where the potential for essential ecosystem services is maintained across both systems but is facilitated by distinct, habitat-adapted specialists. This was most evident in fungi, where management-driven shifts in taxonomy were tightly coupled to functional capacity. Moreover, challenging the prevailing ecological theory that stress simplifies networks, we found that conventional fungal communities were paradoxically more complex, forming a rigid Stress-Clique of co-dependent survivors, while organic bacterial networks were more modular. This structural divergence provides a new mechanistic framework for rhizosphere assembly. We also showed that the host scion’s recruitment of fungi is entirely dependent on the management backdrop, while bacterial recruitment is not. These findings reveal that microbiome-optimized breeding should be conducted within the management framework of the intended production system.</p>